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Continuous evolution of Bacillus thuringiensis toxins overcomes insect resistance

Author

Listed:
  • Ahmed H. Badran

    (Harvard University
    Howard Hughes Medical Institute, Harvard University)

  • Victor M. Guzov

    (Monsanto Company, 245 First Street, Suite 200)

  • Qing Huai

    (Monsanto Company, 245 First Street, Suite 200)

  • Melissa M. Kemp

    (Monsanto Company, 245 First Street, Suite 200)

  • Prashanth Vishwanath

    (Monsanto Company, 245 First Street, Suite 200)

  • Wendy Kain

    (Cornell University)

  • Autumn M. Nance

    (Monsanto Company, 700 Chesterfield Parkway West)

  • Artem Evdokimov

    (Monsanto Company, 700 Chesterfield Parkway West
    † Present address: HarkerBIO, 700 Ellicott Street, Buffalo, New York 14023, USA.)

  • Farhad Moshiri

    (Monsanto Company, 700 Chesterfield Parkway West)

  • Keith H. Turner

    (Monsanto Company, 700 Chesterfield Parkway West)

  • Ping Wang

    (Cornell University)

  • Thomas Malvar

    (Monsanto Company, 700 Chesterfield Parkway West)

  • David R. Liu

    (Harvard University
    Howard Hughes Medical Institute, Harvard University)

Abstract

The Bacillus thuringiensis δ-endotoxins (Bt toxins) are widely used insecticidal proteins in engineered crops that provide agricultural, economic, and environmental benefits. The development of insect resistance to Bt toxins endangers their long-term effectiveness. Here we have developed a phage-assisted continuous evolution selection that rapidly evolves high-affinity protein–protein interactions, and applied this system to evolve variants of the Bt toxin Cry1Ac that bind a cadherin-like receptor from the insect pest Trichoplusia ni (TnCAD) that is not natively bound by wild-type Cry1Ac. The resulting evolved Cry1Ac variants bind TnCAD with high affinity (dissociation constant Kd = 11–41 nM), kill TnCAD-expressing insect cells that are not susceptible to wild-type Cry1Ac, and kill Cry1Ac-resistant T. ni insects up to 335-fold more potently than wild-type Cry1Ac. Our findings establish that the evolution of Bt toxins with novel insect cell receptor affinity can overcome insect Bt toxin resistance and confer lethality approaching that of the wild-type Bt toxin against non-resistant insects.

Suggested Citation

  • Ahmed H. Badran & Victor M. Guzov & Qing Huai & Melissa M. Kemp & Prashanth Vishwanath & Wendy Kain & Autumn M. Nance & Artem Evdokimov & Farhad Moshiri & Keith H. Turner & Ping Wang & Thomas Malvar &, 2016. "Continuous evolution of Bacillus thuringiensis toxins overcomes insect resistance," Nature, Nature, vol. 533(7601), pages 58-63, May.
    • Handle: RePEc:nat:nature:v:533:y:2016:i:7601:d:10.1038_nature17938
    DOI: 10.1038/nature17938
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    Cited by:

    1. Paul Vincelli, 2016. "Genetic Engineering and Sustainable Crop Disease Management: Opportunities for Case-by-Case Decision-Making," Sustainability, MDPI, vol. 8(5), pages 1-22, May.
    2. Mary S. Morrison & Tina Wang & Aditya Raguram & Colin Hemez & David R. Liu, 2021. "Disulfide-compatible phage-assisted continuous evolution in the periplasmic space," Nature Communications, Nature, vol. 12(1), pages 1-14, December.

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